Sister species, shared and divergent responses: early transcriptomic profiling of Bursaphelenchus xylophilus exposed to Esteya spp.

Bursaphelenchus xylophilus, commonly known as the pinewood nematode (PWN), reacts transcriptionally to nematophagous fungi. However, the initial stages leading up to cuticle penetration are not well understood, and it is unclear if closely related fungal antagonists trigger similar responses. In this study, PWN's transcriptomic reactions to Esteya floridanum V14639 (EF) and E. vermicola CCF3117 (EV) were examined at one hour post-inoculation (hpi), capturing the early stages of host-fungus interaction.

Although these fungi are closely related, they produced somewhat different host responses at the 1 hpi mark. EF activated a wide-ranging transcriptional response marked by an increase in peptidase activity and lysosomal pathways, and a decrease in cuticle structural components. Conversely, EV produced a narrower response, without the increased proteolytic and lysosomal activity seen with EF.

When the effects of the two fungi were directly compared, no significantly enriched Gene Ontology categories were found, although pathway analysis did identify DNA replication and repair pathways, with more genes expressed under EF. Enrichment analyses showed a shared transcriptional signature in both interactions, characterized by the downregulation of xenobiotic- and central carbon-metabolism pathways, indicating an early reduction in the nematode's ability to detoxify xenobiotics rather than an induction of detoxification programs.

These results suggest that phylogenetic closeness does not guarantee similar early transcriptional responses, even though comparisons of single isolates cannot differentiate species-level from isolate-level effects.